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Imitation of novel and well-known actions: the role of short-term memory.

Four experiments were carried out using the action span paradigm. In experiment 1 we found that well-learnt, meaningful (MF) actions were imitated better than novel, meaningless (ML) actions. In experiments 2 and 3, during the encoding of MF and ML actions, participants were required to carry out different suppression tasks. In experiment 2 we replicated the advantage of MF actions over ML actions and also found that the motor suppression shortened the action span more than the other forms of suppressions (spatial and articulatory). Action encoding and motor suppression tapping the same subsystem, temporarily holding the motor information, could explain the reduced motor span obtained in experiment 2. Two alternative explanations that could have accounted for this effect were ruled out in experiments 3 and 4. In experiment 3 we verified whether the reduction of the action span was produced by the different combination of the articulatory suppression with motor suppression or with the spatial suppression. In experiment 4, we demonstrated that the reduction was not due to the motor suppression being more difficult than the other types of suppression. The critical finding that the spans of well-learnt, MF actions are longer than those of novel, ML actions observed in experiments 1 and 2 was interpreted in terms of different processing routes engaged in the imitation of these two types of actions. MF actions can be imitated along both a semantic, indirect route and a direct route leading from the visual analysis of the action to the motor system. In contrast, the imitation of ML actions is accomplished along the direct route only.

Brain↗

Is human imitation based on a mirror-neurone system? Some behavioural evidence.

Recently, a population of neurones was discovered in the monkey's ( Macaca nemestrina) ventrolateral part of the pre-motor cortex (area F5). It is specialised for recognising object-oriented actions, regardless of whether these actions are performed or observed by the monkey. The latter observation led to the term mirror-neurones, and because these cells respond to both observed and executed actions, it seems likely that neurones of that type became co-opted during hominid evolution to serve the imitative behaviours that are so prevalent in our species. There is recent physiological evidence that Broca's area, the human ( Homo sapiens) homologue of monkey's area F5, is involved in the imitation of finger movements. However, concluding that human imitation is based on a mirror-neurone system is premature, because: (1) imitation in monkeys does not reach the same level as in humans or apes and (2) monkeys' mirror-neurones are specialised for object-oriented actions. This specialisation has not yet been demonstrated in adult humans. We investigated the role of objects in human imitation behaviour in a response time experiment. Subjects had to imitate downward movements of an index finger. In one condition, the observed finger touched one of two dots either ipsi- or contralaterally. In the other condition, the very same movements had to be imitated. However, there were no dots on the table. The presence of dots had a decisive influence on error patterns and on response times, but did not influence the movement proper. Dots specifically reduced the onset latency of ipsilateral finger movements and they specifically increased the use of the wrong finger, when contralateral movements were required. In general, results showed that objects also drive human imitation behaviour. Hence, it is very likely that imitation emerged from the mirror-neurone system of the common ancestor of monkeys and humans.

Adult↗

Lateralization in motor facilitation during action observation: a TMS study.

Action observation facilitates corticospinal excitability. This is presumably due to a premotor neural system that is active when we perform actions and when we observe actions performed by others. It has been speculated that this neural system is a precursor of neural systems subserving language. If this theory is true, we may expect hemispheric differences in the motor facilitation produced by action observation, with the language-dominant left hemisphere showing stronger facilitation than the right hemisphere. Furthermore, it has been suggested that body parts are recognized via cortical regions controlling sensory and motor processing associated with that body part. If this is true, then corticospinal facilitation during action observation should be modulated by the laterality of the observed body part. The present study addressed these two issues using TMS for each motor cortex separately as participants observed actions being performed by a left hand, a right hand, or a control stimulus on the computer screen. We found no overall difference between the right and left hemisphere for motor-evoked potential (MEP) size during action observation. However, when TMS was applied to the left motor cortex, MEPs were larger while observing right hand actions. Likewise, when TMS was applied to the right motor cortex, MEPs were larger while observing left hand actions. Our data do not suggest left hemisphere superiority in the facilitating effects of action observation on the motor system. However, they do support the notion of a sensory-motor loop according to which sensory stimulus properties (for example, the image of a left hand or a right hand) directly affect motor cortex activity, even when no motor output is required. The pattern of this effect is congruent with the pattern of motor representation in each hemisphere.

Adult↗

Planning and drawing complex shapes.

Arm and hand movements are generally controlled using a combination of sensory-based and memory-based guidance mechanisms. This study examined similarities and differences in visually-guided and memory-guided arm movements, and sought to determine as to what extent certain control principles apply to each type of movement. In particular, the 2/3 power law is a principle that appears to govern the formation of complex, curved hand trajectories; it specifies that the tangential velocity should be proportional to the radius of curvature raised to an exponent of 1/3. A virtual reality system was used to project complex target paths in three-dimensional (3D) space. Human subjects first tracked (with the tip of a handheld pen) a single target moving along an unseen path. The entire target path then became visible and the subject traced the shape. Finally, the target shape disappeared and the subject was to draw it, in the same 3D space, from memory. Most aspects of the movements (speed, path size, shape and arm postures) were very similar across the three conditions. However, subjects adhered to the 2/3 power law most closely in the tracing condition, when the entire target path was visible. Also, only within the tracing condition, there were significant differences in the value of the exponent depending on the size and the spatial orientation of the trajectory. In the tracking and drawing conditions, the exponent was greater than 1/3, indicating that subjects spent more time in areas of tight curvature. This may represent a strategy for learning and remembering the complex shape.

Adult↗

Role of the right dorsal premotor cortex in "physiological" mirror EMG activity.

A distributed cortical network enables the lateralization of intended unimanual movements, i.e., the transformation from a default mirror movement to a unimanual movement. Little is known about the exact functional organization of this "non-mirror transformation" network. Involvement of the right dorsal premotor cortex (dPMC) was suggested because its virtual lesion by high-frequency repetitive transcranial magnetic stimulation (rTMS) increased the excitability of the left primary motor cortex (M1) during unilateral isometric contraction of a left hand muscle (Cincotta et al., Neurosci Lett 367: 189-93, 2004). However, no behavioural effects were observed in that experimental protocol. Here we tested behaviourally twelve healthy volunteers to find out whether focal disruption of the right dPMC by "off-line" One Hz rTMS (900 pulses, 115% of resting motor threshold) enhances "physiological" mirroring. This was measured by an established protocol (Mayston et al., Ann Neurol 45: 583-94, 1999) that quantifies the mirror increase in the electromyographic (EMG) level in the isometrically contracting abductor pollicis brevis (APB) muscle of one hand during brief phasic contractions performed with the APB of the other hand. Mirroring in the right APB significantly increased after real rTMS of the right dPMC. In contrast, no change in mirroring was seen with sham rTMS of the right dPMC, real rTMS of the right M1, or real rTMS of the left dPMC. These findings strongly support the hypothesis that the right dPMC is part of the non-mirror transformation cortical network.

Action Potentials↗

Corticomotor facilitation associated with observation, imagery and imitation of hand actions: a comparative study in young and old adults.

In the present report, we extent our previous findings (Clark et al. in Neuropsychologia 42:105-122, 2004) on corticomotor facilitation associated with covert (observation and imagery) and overt execution (action imitation) of hand actions to better delineate the selectivity of the effect in the context of an object-oriented action. A second aim was to examine whether the pattern of facilitation would be affected by age. Corticomotor facilitation was determined in two groups of participants (young n = 21, 24 +/- 2 years; old n = 19, 62 +/- 6 years) by monitoring changes in the amplitude and latency of motor evoked potentials (MEPs) elicited in hand muscles by transcranial magnetic stimulation. MEP responses were measured from both the first dorsal interosseous (FDI, task selective muscle) and the abductor digiti minimi (ADM) of the right hand while participants attended to four different video presentations. Each of four videos provided specific instructions for participants to either: (1) close their eyes and relax (REST), (2) observe the action attentively (OBS), (3) close their eyes and mentally simulate the action (IMAG), or (4) imitate the action (IMIT). The action depicted in the videos represented a male subject cutting a piece of material with scissors. In the young group, the pattern of results revealed selective facilitation in the FDI in conditions involving either covert (OBS and IMAG) or overt action execution (IMIT). In the ADM, only overt execution with action imitation was associated with significant MEP facilitation. In the old group, a similar pattern of results was observed, although the modulation was less selective than that seen in the young group. In fact, older individuals often exhibited concomitant facilitation in both the FDI and ADM during either covert (OBS and IMAG conditions) or overt action execution (IMIT condition). Taken together, these results further corroborate the notion that the corticomotor system is selectively active when actions are covertly executed through internal simulation triggered by observation or by motor imagery, as proposed by Jeannerod (Neuroimage 14:S103-S109, 2001). With aging, the ability to produce corticomotor facilitation in association with covert action execution appears to be largely preserved, although there seems to be a loss in selectivity. This lack of selectivity may, in turn, reflect age-related alterations in the function of the corticospinal system, which may impair the ability to individuate finger movements either in the covert or overt stage of action execution.

Adult↗

Observation of a finger or an object movement primes imitative responses differentially.

Behavioural advantages for imitation of human movements over movements instructed by other visual stimuli are attributed to an 'action observation-execution matching' (AOEM) mechanism. Here, we demonstrate that priming/exogenous cueing with a videotaped finger movement stimulus (S1) produces specific congruency effects in reaction times (RTs) of imitative responses to a target movement (S2) at defined stimulus onset asynchronies (SOAs). When contrasted with a moving object at an SOA of 533 ms, only a human movement is capable of inducing an effect reminiscent of 'inhibition of return' (IOR), i.e. a significant advantage for imitation of a subsequent incongruent as compared to a congruent movement. When responses are primed by a finger movement at SOAs of 533 and 1,200 ms, inhibition of congruent or facilitation of incongruent responses, respectively, is stronger as compared to priming by a moving object. This pattern does not depend on whether S2 presents a finger movement or a moving object, thus effects cannot be attributed to visual similarity between S1 and S2. We propose that, whereas both priming by a finger movement and a moving object induces processes of spatial orienting, solely observation of a human movement activates AOEM. Thus, S1 immediately elicits an imitative response tendency. As an overt imitation of S1 is inadequate in the present setting, the response is inhibited which, in turn, modulates congruency effects.

Adult↗

The preparation, execution and suppression of copied movements in the human brain.

We used positron emission tomography (PET) to measure movement set-related changes in regional cerebral blood flow (rCBF) when human subjects were asked to copy hand movements. Movement set-related activity in the brain is thought to reflect the processes of movement selection, preparation and inhibition. Four conditions were used. In the first condition, prepare and execute (PE), the hand stimulus to be copied was shown to subjects 3 s before an auditory "go"-cue instructed subjects to execute the movement; a large part of the scanning time was therefore spent in preparing to move. In the immediate execution condition (E), the hand stimulus and the go cue were presented simultaneously. The prepare-only condition (P) was similar to PE, except subjects only prepared to make the movement and did not actually execute any movement when they heard the auditory go-cue. The same stimuli were presented in a baseline condition (B), but the subjects were instructed to neither prepare nor execute movements. There were 5 principle findings: (1) In contrast to a previous study of human set-related activity in which movements were instructed by an arbitrary pattern of LEDs, preparing to make a copied movement causes rCBF changes in area 44 in posterior Broca's area; (2) set-related activity can be recorded in the cerebellar hemispheres and midline; (3) we confirmed that the supramarginal gyrus has a general role in preparing movements - there was more rCBF in the P than the E condition; (4) the cerebellar nuclei and the basal ganglia may be particularly involved in the initiation and execution of a planned movement; these regions were more active in the PE condition than the P condition; (5) the ventrolateral prefrontal cortex and a left anterior cingulate area are part of a distributed system involved in the suppression of a motor response; these areas were significantly more active in the P than the PE condition.

Adult↗

Innate and learned perceptual abilities in the newborn infant.

From research carried out over the last few years, it has become apparent that the visual world of the newborn baby (0-7 days from birth) is highly organised. It is also clear that the newborn infant is an extremely competent learner. These themes are illustrated with respect to two areas of research, face perception and intermodal learning. Evidence is presented suggesting that the human face is "special" in that newborns respond to them as faces, rather than merely collections of stimulus elements. Additional evidence is presented which demonstrates that newborns can form auditory-visual associations after only a short exposure to the stimulation. These lines of evidence suggest that innate capacities, or modules, facilitate and direct early learning in order to allow newborn infants to understand their newly encountered world.

Humans↗

Towards quantification of vocal imitation in the zebra finch.

The transition from an amorphous subsong into mature song requires a series of vocal changes. By tracing song elements during development, we have shown that the imitation trajectory to the target could not be predicted based on monotonic progression of vocal changes, indicating an internal component that imposes constraints on song development. Here we further examine the nature of constraints on song imitation in the zebra finch. We first present techniques for identifying and tracing distinctive vocal changes, and then we examine how sequences of vocal change are expressed and coordinated. Examples suggest two types of constraints on song imitation, based on the nature of the temporal context. Developmentally diachronic constraints are imposed by sequential dependencies between vocal changes as a function of developmental time, whereas developmentally synchronic constraints are given by the acoustic context of notes within the song. Finally, we show that the tendency of birds to copy certain sounds in the song model before others might be related to such constraints. We suggest that documenting the full range of distinctive vocal changes and the coordination of their expression would be useful for testing mechanisms of vocal imitation.

Acoustic Stimulation↗

Bilateral LMAN lesions cancel differences in HVC neuronal recruitment induced by unilateral syringeal denervation. Lateral magnocellular nucleus of the anterior neostriatum.

Twenty-six-day-old male zebra finches received (1) unilateral section of their tracheosyringeal nerve, (2) bilateral lesions of the lateral magnocellular nucleus of the anterior neostriatum (LMAN), and (3) both operations. All birds were kept with an adult, singing male as a tutor until day 65. Tracheo-syringeal nerve-cut birds were able to imitate this model, but LMAN-lesioned birds were not. Bromodeoxyuridine, a marker of cell division, was injected intramuscularly during post-hatching days 61-65 and all birds were killed at 91 days of age. The number of bromodeoxyuridine+ neurons in the high vocal center of the tracheosyringeal-cut birds was twice as high in the intact as in the nerve cut side. This asymmetry disappeared when nerve section was combined with bilateral LMAN lesions. The latter operation, by itself, had no effect on new neuron counts. We suggest that the single nerve cut produced a hemispheric asymmetry in learning, reflected in new neuron recruitment, which disappeared when LMAN lesions blocked learning.

Age Factors↗

Eye direction aftereffect.

Three experiments using computer-generated human figures showed that after a prolonged observation of eyes looking to the left (or right), eyes looking directly toward the viewer appeared directed to the right (or left). Observation of an arrow pointing left or right did not induce this aftereffect on the perceived eye direction. Happy faces produced the aftereffect more effectively than surprised faces, even though the image features of the eyes were identical for both the happy and the surprised faces. These results suggest that the eye direction aftereffect may reflect the adaptation of relatively higher-level mechanisms analyzing the other's eye direction.

Adult↗

Action-effect anticipation in infant action control.

There is increasing evidence that action effects play a crucial role in action understanding and action control not only in adults but also in infants. Most of the research in infants focused on the learning of action-effect contingencies or how action effects help infants to infer goals in other persons' actions. In contrast, the present research aimed at demonstrating that infants control their own actions by action-effect anticipation once they know about specific action-effect relations. About 7 and 9-month olds observed an experimenter demonstrating two actions that differed regarding the action-effect assignment. Either a red-button press or a blue-button press or no button press elicited interesting acoustical and visual effects. The 9-month olds produced the effect action at first, with shorter latency and longer duration sustaining a direct impact of action-effect anticipation on action control. In 7-month olds the differences due to action-effect manipulation were less profound indicating developmental changes at this age.

Association Learning↗

Imitation and language abilities in adolescents with Autism Spectrum Disorder without language delay.

INTRODUCTION: Difficulties imitating gestures have been found in several studies in children and adolescents with Autism Spectrum Disorders (ASD). It has been hypothesized that imitation abilities might be precursors of language abilities in young children with autism. No study on imitation and language abilities in adolescents with ASD has been performed to date. METHODS: Fifteen male adolescents with ASD, 16 male and 13 female controls were compared regarding imitation abilities of upper and lower facial movements, and language skills as assessed by the pragmatic rating scale and the Aachen Aphasia test (AAT). RESULTS: Autism Spectrum Disorder subjects showed reduced imitation abilities of facial movements and non-meaningful combined hand-and-finger gestures. Regarding language, ASD subjects showed difficulties in AAT spontaneous speech measures and reduced pragmatic language abilities. Correlations of imitation and language measures differed between ASD, male and female controls. CONCLUSION: The weak and differential correlations of imitation and language measures in the three comparison groups might imply a differential organization of language and imitation networks in the three comparison groups. Pragmatic abilities, which are a central feature in ASD, were not related to imitation abilities. Therefore, imitation and language abilities in ASD might not be as closely correlated as previously expected.

Adolescent↗

Representing tools: how two non-human primate species distinguish between the functionally relevant and irrelevant features of a tool.

Few studies have examined whether non-human tool-users understand the properties that are relevant for a tool's function. We tested cotton-top tamarins (Saguinus oedipus) and rhesus macaques (Macaca mulatta) on an expectancy violation procedure designed to assess whether these species make distinctions between the functionally relevant and irrelevant features of a tool. Subjects watched an experimenter use a tool to push a grape down a ramp, and then were presented with different displays in which the features of the original tool (shape, color, orientation) were selectively varied. Results indicated that both species looked longer when a newly shaped stick acted on the grape than when a newly colored stick performed the same action, suggesting that both species perceive shape as a more salient transformation than color. In contrast, tamarins, but not rhesus, attended to changes in the tool's orientation. We propose that some non-human primates begin with a predisposition to attend to a tool's shape and, with sufficient experience, develop a more sophisticated understanding of the features that are functionally relevant to tools.

Animals↗

Behavioural development in a matching-to-sample task and token use by an infant chimpanzee reared by his mother.

We investigated the behavioural and cognitive development of a captive male infant chimpanzee, Ayumu, raised by his mother, Ai. Here we report Ayumu's achievements up to the age of 2 years and 3 months, in the context of complex computer-controlled tasks. From soon after birth, Ayumu had been present during an experiment performed by his mother. The task consisted of two phases, a matching-to-sample task in which she received token rewards, and the insertion of these tokens into a vending machine to obtain food rewards. Ayumu himself received no reward or encouragement from humans for any of the actions he exhibited during the experiment. At the age of 9 months and 3 weeks, Ayumu performed his first matching-to-sample trial. At around 1 year and 3 months, he began to perform them consistently. Also during this period, he frequently stole food rewards from his mother. At 2 years and 3 months, Ayumu succeeded for the first time in inserting a token into the vending machine. Once he had succeeded in using a token, he performed both phases of the task in sequence 20 times consecutively. The infant's behaviour was not shaped by food rewards but by a strong motivation to copy his mother's behaviour. Our observations of Ayumu thus mirror the learning processes shown by wild chimpanzees.

Animals↗

Imitation recognition in a captive chimpanzee (Pan troglodytes).

This study investigated the ability of a captive chimpanzee (Pan troglodytes) to recognise when he is being imitated. In the experimental condition of test 1a, an experimenter imitated the postures and behaviours of the chimpanzee as they were being displayed. In three control conditions the same experimenter exhibited (1) actions that were contingent on, but different from, the actions of the chimpanzee, (2) actions that were not contingent on, and different from, the actions of the chimpanzee, or (3) no action at all. The chimpanzee showed more "testing" sequences (i.e., systematically varying his actions while oriented to the imitating experimenter) and more repetitive behaviour when he was being imitated, than when he was not. This finding was replicated 4 months later in test 1b. When the experimenter repeated the same actions she displayed in the experimental condition of test 1a back to the chimpanzee in test 2, these actions now did not elicit those same testing sequences or repetitive behaviours. However, a live imitation condition did. Together these results provide the first evidence of imitation recognition in a nonhuman animal.

Animals↗